UNIVERSITI PUTRA MALAYSIA
EVALUATION OF NEUROBEHAVIORAL AND NEUROTOXICITY EFFECTS OF CHRONIC EMBRYONIC HEAVY METAL EXPOSURE ON
ZEBRAFISH (Danio rerio F. HAMILTON, 1822) LARVAE
NORAINI BINTI ABU BAKAR
FS 2017 34
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HT UPMEVALUATION OF NEUROBEHAVIORAL AND NEUROTOXICITY
EFFECTS OF CHRONIC EMBRYONIC HEAVY METAL EXPOSURE ON ZEBRAFISH (Danio rerio F. HAMILTON, 1822) LARVAE
By
NORAINI BINTI ABU BAKAR
Thesis Submitted to the School of Graduate Studies, Universiti Putra Malaysia, in Fulfilment of the Requirements for the degree of Master of
Science
May 2017
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Commercial use of material may only be made with the express, prior, written
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Copyright © Universiti Putra Malaysia
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Abstract of thesis presented to the Senate of Universiti Putra Malaysia in
fulfillment of the requirement for the degree of Master of Science
EVALUATION OF NEUROBEHAVIORAL AND NEUROTOXICITY EFFECTS OF CHRONIC EMBRYONIC HEAVY METAL EXPOSURE ON
ZEBRAFISH (Danio rerio F. HAMILTON, 1822) LARVAE
By
NORAINI ABU BAKAR
May 2017
Chair: Wan Norhamidah Wan Ibrahim, PhD Faculty: Science
Occurrence of industrialization without environmental care lead to heavy metals
[Mercury chloride (HgCl2), Arsenic trioxide (As2O3)] contamination and caused
adverse effects to human, especially vulnerable to developing fetus and children.
Developmental exposures to heavy metals have been linked to impair motor and
cognitive functions. However, the gap of knowledge to link between
developmental exposure to heavy metal and neurodevelopmental disorders are still
present. Thus, we used zebrafish to demonstrate the neurobehavioral and
neurotoxic effects associated with the chronic embryonic exposure to low concentration of mercury and arsenic in a nanomolar to micromolar concentrations.
The embryos were exposed to different range of HgCl2 (7.5-250 nM) and As2O3
(20-50 μM) starting from 5 hpf until 72 hpf (hatching) in a semi-static condition.
The mortality rate was increased in a dose dependent manner for both
neurotoxicants. Exposure to 100 nM HgCl2 and 30 μM As2O3 decreased the
number of tail coilings, heartbeat, and swimming activity. The adverse effects of
heavy metals on the development of anxiety-related behavior were assessed in 6
dpf larvae. No changes in thigmotaxis upon HgCl2 and As2O3 exposure were
found. Yet, HgCl2 exposures reduced swimming speed and elicit resting while
As2O3 exposure does not elicit any significant changes. Furthermore, aversive
stimulation used to provoke anxiety responses also does not elicit any changes in
thigmotaxis and avoidance response for both neurotoxicants. Overall, alteration in motor and anxiety responses were also linked with the increased apoptosis assessed
at different time points. The peaks were shifted for both neurotoxicants whereby
reaching an early peak at 24 hpf as compared to the control (72 hpf). Exposure to
both neurotoxicants affects biochemical status (proteins, lipids, carbohydrates and
nucleic acids) of the zebrafish larvae. These results showed that HgCl2 and As2O3
exert its toxic effects at cellular and biochemical level that leading to alteration at
behavioral level.
Keywords : zebrafish; mercury chloride; arsenic trioxide; locomotor; anxiety
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Abstrak tesis yang dikemukakan kepada Senat Universiti Putra Malaysia
Sebagai memenuhi keperluan untuk ijazah Sarjana Sains
PENILAIAN KESAN TINGKAHLAKU-NEURO DAN NEUROTOKSIK AKIBAT DEDAHAN KRONIK LOGAM BERAT TERHADAP LARVA
ZEBRAFISH (Danio rerio F. HAMILTON, 1822)
Oleh
NORAINI ABU BAKAR
Mei 2017
Pengerusi: Wan Norhamidah Wan Ibrahim, PhD Fakulti: Sains
Aktiviti perindustrian tanpa menitikberatkan penjagaan alam sekitar menyumbang
kepada pencemaran logam berat [Merkuri klorida (HgCl2), Arsenik trioksida
(As2O3)] dan menyebabkan kesan buruk kepada manusia terutama kepada
perkembangan janin dan kanak-kanak. Dedahan jangka panjang kepada logam
berat telah dikaitkan dengan kemerosoton fungsi motor dan kognitif. Walau
bagaimanapun, jurang pengetahuan untuk menghubungkaitkan antara dedahan
logam berat dan gangguan perkembangan-neuro masih lagi wujud. Oleh itu, kami
menggunakan zebrafish untuk mengkaji kesan tingkah laku-neuro dan neurotoksik
akibat dedahan kepada merkuri dan arsenik pada kepekatan rendah secara kronik
dari kepekatan nanomolar sehingga kepekatan mikromolar. Embrio didedahkan
kepada kepekatan berbeza HgCl2 (7.5-250 nM) dan As2O3 (20-50 μM) bermula dari 5 hpf sehingga 72 hpf (penetasan) dalam keadaan semi-statik. Kadar kematian
telah meningkat sejajar dengan peningkatan dos untuk kedua-dua neurotoksikan.
Dedahan 100 nM HgCl2 dan 30 μM As2O3 mengakibatkan penurunan bilangan
pusingan ekor, degupan jantung, dan aktiviti renang. Kesan buruk logam berat
kepada tingkah laku kebimbangan dilakukan pada larva berumur 6 dpf. Tiada
perubahan dalam thigmotaksis ditemui selepas larva didedahkan dengan HgCl2 dan
As2O3. Namun, dedahan HgCl2 menyebabkan penurunan kelajuan renang dan
peningkatan tingkah laku rehat manakala dedahan As2O3 tidak menghasilkan
perubahan yang ketara. Tambahan pula, simulasi aversif yang digunakan untuk
menguji tindakbalas kebimbangan juga tidak menghasilkan perubahan terhadap
thigmotaksis dan tindakbalas mengelak untuk kedua-dua neurotoksikan. Secara
keseluruhan, perubahan fungsi motor dan tindakbalas kebimbangan juga dikaitkan dengan peningkatan apoptosis yang dinilai pada masa yang berbeza. Kedua-dua
neurotoksikan mengakibatkan perubahan posisi puncak apoptosis di mana puncak
apoptosis dicapai lebih awal pada 24 hpf berbanding kawalan yang mencapai
puncak apoptosis pada 72 hpf. Dedahan kepada kedua-dua neurotoksikan turut
memberi kesan terhadap status biokimia (protein, lipid, karbohidrat dan asid
nukleik) larva zebrafish. Penemuan ini membuktikan bahawa HgCl2 dan As2O3
memberi kesan toksik pada peringkat selular dan biokimia yang juga membawa
kepada perubahan di peringkat tingkah laku.
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Kata kunci: zebrafish; merkuri klorida; arsenic trioksida; lokomotor; kebimbangan
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ACKNOWLEDGEMENTS
First and foremost, Alhamdulillah for giving me strength, patience, courage and
determination in completing this master degree project. All grace and thanks
belong to Almighty Allah S.W.T. I would like to acknowledge Jabatan
Perkhimatan Awam (JPA) for sponsorship throughout my studies. I also like to
convey my greatest gratitude to my dearest supervisor, Dr. Wan Norhamidah Wan
Ibrahim, for her invaluable advice, helpful guidance and who always provides
valuable recommendations and suggestions to my inquiries tranquilly and accurately. Her great ideas, suggestion and expertise are sincerely and highly
appreciated. I would also like to express my sincere appreciation to my teammates,
Nurul Farhana Ramlan and Nurul Syafida Mohd Sata, Dr. Che Azurahanim Che
Abdullah and everyone involved for their valuable assistance, advice and patient
throughout this master project.
My special appreciation and thank you to my beloved family, for their blessing,
sacrifices and encouragement throughout this master project. Finally, my greatest
thanks are to my co-supervisor, Dr. Syaizwan Zahmir Zulkifli, all lecturer of
Biology Department,UPM, colleagues and staffs in UPM, who helped me and wish
to extend my sincere appreciation and the best wishes.
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This thesis was submitted to the Senate of Universiti Putra Malaysia and has been
accepted as fulfillment of the requirement for the degree of Master of Science. The
members of the Supervisory Committee were as follows:
Wan Norhamidah Wan Ibrahim, PhDSenior Lecturer
Faculty of Science
Universiti Putra Malaysia
(Chairman)
Syaizwan Zahmir Zulkifli, PhDSenior Lecturer
Faculty of Science
Universiti Putra Malaysia
(Member)
__________________________
ROBIAH BINTI YUNUS, PhD Professor and Dean
School of Graduate Studies
Universiti Putra Malaysia
Date:
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Declaration by graduate student
I hereby confirm that:
� this thesis is my original work;
� quotation, illustrations and citations have been duly referenced;
� this thesis has not been submitted previously or concurrently for any other
degree at any other institutions;
� intellectual property from the thesis and copyright of thesis are fully-owned by
Universiti Putra Malaysia, as according to the Universiti Putra Malaysia
(Research) Rules 2012;
� written permission must be obtained from the supervisor and the office of
Deputy Vice-Chancellor (Research and Innovation) before thesis is published
(in the form of written, printed or in electronic form) including books, journals,
modules, proceedings, popular writings, seminar papers, manuscripts, posters,
reports, lecture notes, learning modules or any other materials as stated in the
Universiti Putra Malaysia (Research) Rules 2012;
� there is no plagiarism or data falsification/fabrication in the thesis, and
scholarly integrity is upheld as according to the Universiti Putra Malaysia(Graduate Studies) Rules 2003 (Revision 2012-2013) and the Universiti Putra
Malaysia (Research) Rules 2012. The thesis has undergone plagiarism
detection software.
Signature: _________________________ Date:___________________
Name and Matric No.: Noraini Abu Bakar (GS42726)
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Declaration by Members of Supervisory Committee
This is to confirm that:
� the research conducted and the writing of this thesis was under our supervision;
� supervision responsibilities as stated in the Universiti Putra Malaysia (Graduate
Studies) Rules 2003 (Revision 2012-2013) are adhered to.
Signature:
Name of Chairman of
Supervisory
Committee: Dr. Wan Norhamidah Wan Ibrahim
Signature:
Name of Member of
Supervisory
Committee: Dr. Syaizwan Zahmir Zulkifli
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TABLE OF CONTENTS
PageABSTRACT i
ABSTRAK ii
ACKNOWLEDGEMENTS iv
APPROVAL v
DECLARATION vii
LIST OF TABLES �ii
LIST OF FIGURES x���
LIST OF ABBREVIATIONS x��
CHAPTER
1 INTRODUCTION 1
2 LITERATURE REVIEW 3
2.1 Mental health problem 3
2.1.1 Anxiety versus fear 4
2.1.2 The biology of anxiety 5
2.1.3 Relevance of anxiety research 52.2 Animal models of anxiety 6
2.2.1 Zebrafish (Danio rerio) 7
2.2.2 Development of motor function 9
2.2.3 Development of sensory function 10
2.2.3.1 The visual system 11
2.2.3.2 Visual processing and visual
assays
12
2.2.3.3 Development of lateral line 13
2.2.4 Development of cognitive function 14
2.2.5 Regulation of anxiety in zebrafish 15
2.2.6 Thigmotaxis and avoidance response
in zebrafish
16
2.2.7 How thigmotaxis relevant to human 16
2.2.8 Ecological significance of thigmotaxis 16
2.3 Environmental pollutant 17
2.3.1 Physical and chemical properties of
heavy metals
17
2.3.2 Environmental fate of mercury and
arsenic
19
2.3.3 Dietary exposure to mercury and
arsenic at low concentration
20
2.3.4 Mechanism of mercury and arsenic
neurotoxicity
22
2.4 Developmental neurotoxicity 23
2.5 Behavior as endpoints in neurotoxicity research 24
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3 MATERIALS AND METHODS 26
3.1 Fish husbandry and embryos collection 26
3.2 Heavy metals and drugs exposure 28
3.3 Zebrafish teratogenicity evaluation 28
3.4 Larval locomotor assay 29
3.5 Larval anxiety-like responses assay 30
3.6 Detection of apoptosis 34
3.7 Fourier transform infrared spectroscopy (FTIR) 34
3.8 Statistical analysis 34
4 RESULTS 364.1 Toxicity effects of chronic embryonic exposure
to HgCl2 and As2O3
36
4.2 Effect of chronic embryonic exposure to HgCl2
and As2O3 on the spontaneous tail coiling
38
4.3 Effects of HgCl2 and As2O3 on locomotor
activity
40
4.4 Effects of HgCl2 and As2O3 on anxiety-related
responses
42
4.4.1 Effect of HgCl2 on thigmotaxis and
avoidance responses
42
4.4.2 Effect of HgCl2 on the swimming speed and rest
44
4.4.3 Effect of As2O3 on thigmotaxis,
avoidance, speed and rest
46
4.5 Determination of apoptosis in the zebrafish
embryo exposed to HgCl2 and As2O3
48
4.6 Effects of HgCl2 and As2O3 on biochemical
alterations
52
5 DISCUSSION 56
5.1 Toxicity effects of chronic embryonic HgCl2
and As2O3 exposure
56
5.2 Effect of chronic embryonic HgCl2 and As2O3
on spontaneous tail coiling57
5.3 Effects of HgCl2 and As2O3 on locomotor
activity
57
5.4 HgCl2 and As2O3 impaired anxiety-like
responses
59
5.5 Effects of HgCl2 and As2O3 on apoptosis 61
5.6 Biochemical alterations induced by HgCl2 and
As2O3
62
6 SUMMARY, CONCLUSION AND RECOMMENDATIONS FOR FUTURE RESEARCH
63
6.1 Limitation and future perspectives of study 63
6.2 Contribution findings 64
6.3 Conclusion 65
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REFERENCES 66
APPENDICES 85
BIODATA OF STUDENT 98
LIST OF PUBLICATIONS 99
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LIST OF TABLES
Table Page
2.1 Comparison between fear and anxiety 4
2.2 Anxiety assays in different animal models 7
2.3 The differences between human and zebrafish eye 11
2.4 Physical and chemical properties of mercury compounds 18
2.5 Natural and anthropogenic sources of mercury and arsenic 19
2.6 Some of the fish species contaminated with highest level of
mercury.21
2.7 Studies on in vitro bioaccessibility of iAs contained in
different food items21
4.1 General band assignment of the FITR spectra of control,
100 nM HgCl2 and 30 μM As2O3 exposed zebrafish larvae
53
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LIST OF FIGURES
Figure Page
2.1 Morphological differences between male and female zebrafish
(Danio rerio)
8
2.2 Different types of neurons that involved in the locomotor
activity9
2.3 Behaviors exhibit by zebrafish larvae from day 0 until day 6 10
2.4 Eye development in zebrafish from 0 hour post-fertilisation (hpf) until 74 hpf
12
2.5 Development of the posterior lateral line sensory receptors in
developing zebrafish at around 18 hpf until 7 dpf
13
2.6 Development of learning behaviors in zebrafish larvae that
start from 24 hpf until 144 hpf (6 days)
14
2.7 Regulation of anxiety in zebrafish 15
3.1 The equipments used to harvest the zebrafish embryos 27
3.2 Open field test for 6 dpf zebrafish larvae (red arrow) 29
3.3 Anxiety-like responses assay’s setup and its parameters 31
3.4 Automated analysis of larval behavior using ImageJ
ZebraMacro
32
3.5 Microsoft Excel calculation to determine the coordinates of
the larvae
33
4.1 The toxicity effects of HgCl2 and As2O3 37
4.2 Effect of HgCl2 and As2O3 on the tail coiling 39
4.3 Effects of HgCl2 and As2O3 on swimming activity 41
4.4 Behavioural alterations at 6 dpf in response to aversive
stimulus upon 100 nM HgCl2, 100 mg/L caffeine and 5 mg/L
buspirone exposure
43
4.5 The toxicity effects of 100 nM HgCl2, 100 mg/l caffeine and 5
mg/l buspirone on the swimming speed in response to
aversive stimulus
45
4.6 Behavioural alterations at 6 dpf in response to aversive
stimulus upon 30 μM As2O3, 100 mg/l caffeine and 5 mg/l
buspirone exposure
47
4.7 Detection of apoptotic cell death in the 24 hpf zebrafish
embryos
49
4.8 Detection of apoptotic cell death in the 48 hpf zebrafish
embryos
50
4.9 Detection of apoptotic cell death in the 72 hpf zebrafish
embryos
51
4.10 The alterations of the apoptosis upon HgCl2 and As2O3
exposure
52
4.11 The representative FTIR spectra in the 6 dpf zebrafish larvae
upon HgCl2 and As2O3 exposure in the 500-4000 cm-1 region.
55
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LIST OF ABBREVIATIONS
ANOVA
As2O3
ADHD
ASD
CaCl2°C
CNS
dpf
DNT
Na2HPO4
g/cm3
g/L
hr
hpf
kg
HgCl2
MgSO4
MeHg
μg
μg/L
μm
μM
mg/kg
mg/L
mM
min
KH2PO4
ng/g
nM
PNS
pM
KBr
KCl
s
NaAsO2
NaHCO3
NaCl
SEM
t
Analysis of Variance
Arsenic trioxide
Attention Deficit Hyperactivity Disorder
Autism spectrum disorder
Calcium chloride
Celsius
Central Nervous System
Day post fertilisation
Developmental Neurotoxicity Testing
Disodium phosphate
Gram per cubic centimetre
Gram per litre
Hour
Hour post fertilisation
Kilogram
Mercury (II) chloride
Magnesium sulphate
Methylmercury
Microgram
Microgram per litre
Micrometer
Micromolar
Milligram per kilogram
Milligram per litre
Millimolar
Minute
Monopotassium phosphate
Nanogram per gram
Nanomolar
Peripheral nervous system
Picomolar
Potassium bromide
Potassium chloride
Second
Sodium arsenite
Sodium bicarbonate
Sodium chloride
Standard Error Mean
Time
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CHAPTER 1
INTRODUCTION
Mental health problems are projected contributing to 16.8% of the global burden
diseases (WHO, 2006). Currently, Ministry of Health Malaysia reported that
mental health problems keep growing in Malaysia which also affecting children
(KKM, 2015), of particular interest anxiety. The prevalence of the anxiety disorders is increasing worldwide, which the etiology is currently unknown. The
interference of the normal developmental processes in the central nervous system
(CNS) at early stage have been suggested as one of the factors leading to anxiety
disorders (Pamphlett, 2014; Ng et al., 2013; Berk et al., 2011; Yorifuji et al., 2011).
The developing CNS is exclusively sensitive to environmental pollutants as
compared to adults (Lohren et al., 2015; McKean et al., 2015; Ho et al., 2013).
Prenatal exposures to heavy metals have been associated with increased risk of
aggression, depression and behavioral alterations later in life (Guilarte et al., 2012).
Even worst, the emergence of large scale industrial activities over the last decades
have introduced massive amounts of new chemicals into the environment which
led to greater risks of chemical exposure to human. Apparently, these chemicals
and other thousand chemicals available in the commerce are lacking extensive developmental neurotoxicity testing (DNT) data that are crucial for the risk
assessment process for the human (Smirnova et al., 2014; Grandjean & Landrigan,
2006).
In the general population, human can be exposed to different forms of mercury and
arsenic through the contaminated air inhaled, drinking water, food consumed and
cosmetics contaminated with heavy metals (Perez et al., 2017; Ellingson et al.,
2014; Holmes et al., 2009; Clarkson et al., 2003). The fact that different forms of
mercury and arsenic have the ability to accumulate within the human body, and the
developing nervous system is highly sensitive throughout the gestational period, even minute exposure to the inorganic or organic heavy metals can pose persistent
harmful effects to the developing nervous system (ATSDR, 2007; WHO, 2003).
Noteworthy, the biological barriers (blood brain barrier, placental barrier) are
unable to protect the developing nervous system from neurotoxicity effects of
heavy metals. Several epidemiological studies showed that embryonic exposure to
mercury can produce detrimental effects on cognition and psychomotor functions
in the children from infancy to adolescence (Bellinger et al., 2016; Debes et al.,
2006) while exposure to arsenic caused deficit in IQ, loss of motor functions and
developed neuropsychiatric disorders (Yorifuji et al., 2016; Nahar et al., 2014).
Supporting this, experimental evidences in animal models have shown that
exposure to mercury (Huo et al., 2015; Teixeira et al., 2014; Smith et al., 2010) and
arsenic (Mao et al., 2016; Wu et al., 2016) during developmental stages caused neurocognitive and emotional dysfunctions. However, the adverse effects due to
exposure at low concentrations which are more environmentally relevant and
associated with the neurodevelopmental dysfunctions are currently scarce.
Although rodents have been traditionally used as an animal model for DNT testing,
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though, it is proven laborious, high cost for large scale screening and incompatible
to study the effects of chemicals at low concentrations for long term period, thus
caused little progress in the DNT testing.
Therefore, there is recognized requirement to use alternatives non-mammalian
models to support chemicals screening for DNT testing. Zebrafish started to gain
attention as a model of choice for DNT research owing to their special
characteristics. High fecundity of the zebrafish is amenable for high throughput
toxicity approaches which not feasible in the rodents. Shorter embryonic period (3
days) as compared to the rodents (18-28 days) has put the zebrafish at advantage as it minimizes the use of chemicals, cost of the maintenance and less laborious.
Importantly, the high conservation of basic CNS organization with similar key
pathway that relevance to human diseases makes the zebrafish a relevant animal
model for DNT testing (Patten et al., 2014; Howe et al., 2013; Kalueff et al., 2013;
Tsuji & Crofton, 2012; Bal-Price et al., 2010). In this thesis, zebrafish was used as
a model organism in order to understand the neurotoxic and neurobehavioral
alterations after chronic embryonic exposure to HgCl2 and As2O3 at nanomolar and
micromolar concentrations.
The objectives of this project are:
a) To identify the toxic effects of embryonic exposure to HgCl2 and As2O3
during developmental stages of zebrafish (Danio rerio)
b) To examine the alteration in motor function and anxiety-related responses
of zebrafish (Danio rerio) larvae after embryonic exposure to HgCl2 and
As2O3
c) To assess apoptosis in the zebrafish embryos and larvae after embryonic
exposure to HgCl2 and As2O3
d) To evaluate the biochemical changes in the zebrafish embryos and larvae
after embryonic exposure to HgCl2 and As2O3
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